Abstract
The new plant virus family Virgaviridae is described. The family is named because its members have rod-shaped virions (from the Latin virga = rod), and it includes the genera Furovirus, Hordeivirus, Pecluvirus, Pomovirus, Tobamovirus and Tobravirus. The chief characteristics of members of the family are presented with phylogenetic analyses of selected genes to support the creation of the family. Species demarcation criteria within the genera are examined and discussed.
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The International Committee on Taxonomy of Viruses (ICTV) has recently approved a proposal to create a plant virus family Virgaviridae. The family is named because its members have rod-shaped virions (from the Latin virga = rod), and it includes the genera Furovirus, Hordeivirus, Pecluvirus, Pomovirus, Tobamovirus and Tobravirus. The chief characteristics of members of the family are:
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Alpha-like replication proteins that form a distinct phylogenetic “family” [5].
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Single-stranded RNA + sense genomes with a 3′-t-RNA-like structure and no polyA tail.
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Rod-shaped virions 20–25 nm in diameter with a central “canal”.
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Coat proteins of 19–24 kDa.
It contains some viruses in which there is a single cell-to-cell movement protein (MP) of the ‘30K’ superfamily [7] and others that encode a triple gene block (TGB) [8]. There are also differences in the number of genomic RNAs (1, 2 or 3 depending on the genus), but sequence analysis of the polymerase and other genes suggests that the viruses form a coherent taxonomic unit (see below). Some properties of the six genera included in the family are summarized in Table 1, and their genome organization is shown in Fig. 1. Biologically, the viruses are fairly diverse. They have been reported from a wide range of herbaceous and mono- and dicotyledonous plant species, but the host range of individual members is usually limited. All members can be transmitted experimentally by mechanical inoculation, and for those in the genus Tobamovirus, this is the only known means of transmission. In some genera, transmission is by soil-borne vectors, while members of the genus Hordeivirus are transmitted through pollen and seed. The only genus with rod-shaped virions excluded from this list is Benyvirus, because this is much more distantly related in phylogenetic analyses of the polymerase (see below) and because (unlike the others) its members have a polyadenylated genome and a polymerase that is processed by autocatalytic protease activity.
On the basis of their analysis of the RNA-dependent RNA polymerase (RdRp) gene from a wide range of viruses, Koonin and Dolja [5] included viruses from the six genera described in this paper within RdRp Supergroup 3, which they sub-divided into three lineages that they suggested might correspond to orders. One of these lineages, which they named Tobamo, included the six genera considered here, together with the families Closteroviridae and Bromoviridae and the genus Idaeovirus. Phylogenetic analysis (using several different methods) of the RdRp domain, of the whole replication protein or of the fused Methyl transferase–Helicase–RdRp domains continues to support this grouping and shows that the genus Benyvirus is much too distantly related to be grouped in this family (see Fig. 2). The inclusion within the branch of the families Closteroviridae and Bromoviridae also justifies the inclusion of all six genera within the single family Virgaviridae. The replication proteins constitute the majority of the genomes of these viruses and provide the best phylogenetic trees, but there are also indications of relatedness amongst the other genes. For example, the TGB proteins of the genera Hordeivirus, Pecluvirus and Pomovirus are clearly related and form a distinct group separate from those of the genus Benyvirus and the filamentous viruses in the family Flexiviridae (recently split into two families). A tree for TGBp1 sequences is provided in Fig. 3, and more details supporting this classification of the TGB proteins are provided by Morozov and Solovyev [8]. The small size of the coat protein and its inherent variability make it less suitable for phylogenetic analysis. Nevertheless, significant groupings of genera occur (Furo- with Pomo-; Peclu- with Hordei- and Tobra- a bit more distant) which correspond with those found within the RdRp (Fig. 4). There are also close relationships between the small cysteine-rich proteins of Furovirus, Hordeivirus, Pecluvirus and Tobravirus, although those of Pomovirus do not align well with them (data not shown).
The taxonomic structure of the new family and the species currently included are listed in Table 2.
Sequence differences between and within the existing species in the family were examined and compared with molecular criteria for species discrimination provided by the relevant study groups in the 8th ICTV report [2]. Individual pairwise comparisons were therefore made using the nt and aa sequences of each fully sequenced gene from every available accession in the family Virgaviridae contained in the international databases. Comparisons used the GCG [1] program GAP (with a gap creation penalty of 50 and a gap extension penalty of 3 for nt comparisons and values of 8 and 2, respectively, for aa comparisons). This program aligns the two sequences selected and calculates the percentage identity and similarity between them. To assist with the large numbers of comparisons, software was written (Antoniw, unpublished) to generate batch files that were run in GCG and also to extract and summarize data from the output files. Some of the chief features of the data for the replication protein, the RdRp and the coat protein genes are summarized in Table 3. Within some genera, there are rather few species and sequences, but some conclusions may nevertheless be reached. For the genus Tobravirus, it is already known that coat protein sequences (from RNA2) are of little taxonomic value [2], and this appears also to be the case for the genus Pecluvirus. Within the replication protein and RdRp, isolates of the same species usually had >90% nt or aa sequence identity. Comparisons between genera show that some existing species in the genus Tobamovirus are rather closely related and there may be merit in re-examining the species demarcation criteria within this genus.
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Rothamsted Research receives grant-aided support from the Biotechnology and Biological Sciences Research Council of the UK.
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Adams, M.J., Antoniw, J.F. & Kreuze, J. Virgaviridae: a new family of rod-shaped plant viruses. Arch Virol 154, 1967–1972 (2009). https://doi.org/10.1007/s00705-009-0506-6
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DOI: https://doi.org/10.1007/s00705-009-0506-6